Heterotrophic and Autotrophic Microbial Populations in Cold Perennial Springs of the High Arctic

Abstract

The saline springs of Gypsum Hill in the Canadian high Arctic are a rare example of cold springs originating from deep groundwater and rising to the surface through thick permafrost. The heterotrophic bacteria and autotrophic sulfur-oxidizing bacteria (up to 40% of the total microbial community) isolated from the spring waters and sediments were classified into four phyla (Actinobacteria, Bacteroidetes, Firmicutes, and Proteobacteria) based on 16S rRNA gene analysis; heterotrophic isolates were primarily psychrotolerant, salt-tolerant, facultative anaerobes. Some of the isolates contained genes for thiosulfate oxidation (soxB) and anoxygenic photosynthesis (pufM), possibly enabling the strains to better compete in these sulfur-rich environments subject to long periods of illumination in the Arctic summer. Although leucine uptake by the spring water microbial community was low, CO 2 uptake was relatively high under dark incubation, reinforcing the idea that primary production by chemoautotrophs is an important process in the springs. The small amounts of hydrocarbons in gases exsolving from the springs (0.38 to 0.51% CH 4 ) were compositionally and isotopically consistent with microbial methanogenesis and possible methanotrophy. Anaerobic heterotrophic sulfur oxidation and aerobic autotrophic sulfur oxidation activities were demonstrated in sediment slurries. Overall, our results describe an active microbial community capable of sustainability in an extreme environment that experiences prolonged periods of continuous light or darkness, low temperatures, and moderate salinity, where life seems to rely on chemolithoautotrophy.Perennial springs are extremely rare in areas underlain by deep, continuous permafrost, because of the limited opportunity for exchange between sub-and suprapermafrost groundwater systems. The perennial springs found at Gypsum Hill (GH) on west-central Axel Heiberg Island in the Canadian high Arctic originate from deep saline groundwater and rise to the surface through ϳ600-m-thick continuous permafrost in a region with a mean annual temperature of Ϫ15°C (38). They discharge oligotrophic brines (7.5 to 7.9% salt) that are rich in inorganic sulfur compounds, saturated with dissolved gasses (primarily N 2 ), and maintain a constant temperature (Ϫ1.3°C to 6.9°C) throughout the year despite air temperatures that drop below Ϫ40°C during the winter (36, 38). The springs' location at nearly 80 o N exposes them to long periods of continuous illumination or total darkness during the Arctic summer and winter, respectively.Recent reports have examined mesophilic (15) and cold sulfur (14, 22, 23) springs, including cold springs in Germany that harbor a string-of-pearls-like community consisting of microbial filaments of Archaea in close association with sulfideoxidizing bacteria related to Thiothrix (33). Sulfur springs usually support a diversity of sulfur-oxidizing bacteria, including anaerobic anoxygenic phototrophs (purple and green sulfur bacteria) that use reduced sulfur compounds as electron donors...

Microbial characterization of a subzero, hypersaline methane seep in the Canadian High Arctic

“…Although ANME-related microorganisms were not detected in the source pool sediment from other AHI springs, similarities do exist between the bacterial communities of LH to that of CP and GH, including the detection and isolation of Gillisia, Loktanella, Marinobacter, Halomonas and Cytophaga spp. (Perreault et al, 2007(Perreault et al, , 2008. The microbial communities of marine-based methane-seep sediments have been intensively studied due to the phenomenon of AOM undertaken by the ANME group of archaea, typically coupled with sulfate-reducing bacteria (SRB), in these environments (Hinrichs et al, 1999;Michaelis et al, 2002;Hallam et al, 2004;Knittel et al, 2005;Nauhaus et al, 2005;Lloyd et al, 2006).…”

“…Further work identified culturable microbes from the spring sediments with autotrophic and sulfur-oxidation activities (Perreault et al, 2008), and the small amounts of hydrocarbons in gases exsolving from these springs were compositionally and isotopically consistent with microbial methanogenesis and possible methanotrophy (Perreault et al, 2007). Niederberger et al (2009) characterized gray-colored microbial streamers that form during the winter months in the snow-covered regions of the GH spring runoff channels.…”

“…These springs are among the only known cold springs in thick permafrost on Earth (Andersen et al, 2002) and the geomorphology, chemistry, thermal environment and microbiology of two sets of moderately cold, saline springs (Gypsum Hill (GH), Colour Peak (CP)) located at Expedition Fiord on AHI have been extensively studied (Pollard et al, 1999;Andersen et al, 2002;Perreault et al, 2007Perreault et al, , 2008Niederberger et al, 2009). These springs flow throughout the entire year with constant discharge temperatures ranging from À0.5 to 6.9 1C, and discharge waters that are moderately saline (7.5-15.8% salts), anoxic (mean oxido-reduction potential (ORP) of À325 mV), near-neutral (pH 6.9-7.5), rich in both sulfate (2300-3724 mg l À1 ) and sulfide (25-100 p.p.m.)…”

Microbial diversity and activity in hypersaline high Arctic spring channels

“…This medium has been successfully used for culturing and enumerating heterotrophic microorganisms from Arctic hypersaline springs as described in previous studies (Niederberger et al 2010;Perreault et al 2008). All plate counts were performed in triplicate.…”

“…These springs occur in an area with an average annual air temperature of -15°C that can dip below -40°C during the winter months. The microbial communities of two moderately extreme High Arctic spring systems, Gypsum Hill (GH) and Colour Peak (CP) were found to contain active microbial communities capable of existing in an extreme environment that experiences prolonged periods of continuous light or darkness, low temperatures (-1t o8°C), and moderate salinity (*8 to 15%), and where life seems to rely on sulfur-based chemolithoautotrophy Perreault et al 2007Perreault et al , 2008.…”